Abstract

Ectoparasite serves as vector of zoonotic and economic
diseases, and degrades the welfare of animal. A gap of knowledge concerning
ectoparasite fauna has remained in livestock, poultry, companion and exotic
animals in Philippines where limited record existed and none in remote regions
such as in Leyte Island, Philippines. The present study was carried out to
determine the species of lice, fleas and ticks infesting various animals in
Baybay, Leyte. A total of 577 ectoparasites were collected, processed and
identified morphologically. There were 19 different species identified: 14 lice,
2 fleas, and 3 ticks. Chicken lice recorded were Goniocotes gallinae,
Goniodes
dissimilis, Lipeurus caponis, Oxylipeurus dentatus, Menopon gallinae, and
Menacanthus stramineus. Lice isolated from rock pigeon and turkey were
Columbicola columbae and Chelopistes meleagridis, respectively.
Damalinia caprae
and Linognathus spp. were observed in goats; D. ovis in sheep;
Heterodoxus
spinigera in dog; Haematopinus tuberculatus in both carabao and cattle; and
H.
suis in pig. Fleas isolated from dogs were Ctenocephalides felis and
Pulex
irritans, the former was also seen in cat. Rhipicephalus sanguineus,
R.
microplus and Aponomma spp. were recorded from dog, large ruminant and
reticulated python, respectively. Knowledge in ectoparasite distribution and
taxonomic composition will lead to better understanding of vector and
vector-borne diseases. This will result in the improvement of diagnosis,
prevention and control strategies in the region.

Keywords: arthropod vector, ectoparasite, tropical parasite

Introduction

Ectoparasites affect the well-being of animals and serve
as vector of zoonotic and economic diseases. Three of these important
ectoparasites belong to suborder Ixodida (ticks), and orders Siphonaptera
(fleas) and Phthiraptera (lice) (Bowman 2009). Ticks and tick-borne diseases can
cause major production losses in ruminant and threat to public health by
transmitting zoonotic bacteria, viruses and protozoa (Ahmed et al 2007). They
are also nuisance to companion animals causing skin damage and irritation.
Meanwhile, fleas serve as carrier of known human and animal pathogenic
microorganisms such as Yersinia, Rickettsia and Bartonella. They are annoying
biters leading to discomfort, secondary infection and skin allergy (Dieme et al
2015; Wall and Shearer 1997). Lice transmit and serve as reservoir of pathogens
like swinepox and Rickettsia (Wolf 2010).Their chewing and blood feeding habit
will result to anaemia, skin irritation and decrease in production capacity
among poultry and livestock (Wall and Shearer 1997). Therefore, ectoparasites
are serious pest with vital role in disseminating vector-borne diseases,
decreasing animal production and debilitating animal welfare (Campbell-Lendrum
et al 2015; Fuehrer et al 2012).

The distribution of ectoparasites certainly varies by
location and climate. Tropical and subtropical climates favour good habitat for
parasite survival and reproduction, thus infestations are common in Southeast
Asian countries (Changbunjong et al 2009; Petney et al 2007). In the Philippines,
published reports of ectoparasites fauna in domestic and exotic animals are very
few especially in the islands of Visayas. Profile of ectoparasites species (i.e.
lice, fleas and ticks) has focused mainly in wild animals from Luzon Island, the
northern part of the country.

Researchers have isolated lately some old and new
arthropod parasite from Philippine wild birds and small mammals. Common avian
lice of the genus Menacanthus, Goniocotes, Menopon and Lipeurus were reported
from wild birds in a rescue center
(Sia
Su et al 2013). Lice of the genus Columbicola, Auricotes,
Strigiphilus, Colpocephalum, Kurodaia, Pseudomenopon, Rallicola, and
Eulaemobothrionwere found in selected
Philippine wild birds, in which novel lice species were identified (Eduardo
2014; Eduardo 2012; Desemero and Eduardo 2011). Fleas
collected from small mammals belonging to genus Polyplax, Xenopsyllia,
Lentistivalius, Thaumapsylla, Ischnopsyllus, Sigmactenus, and Medwayella with
new characterized species were also reported (Hastriter and Bush 2014; Durden
and Beaucournu 2000; Luyon and Salibay 2007). Moreover, old reports of tick’s
species isolated among Philippine wild pigs, Philippine deer and varanid lizards
were from the genus Dermacentor, Haemaphysalis and Amblyomma, respectively
(Auffenberg 1988; Wassef and Hoogstraal 1988). On the other hand, species of
ectoparasites identified from domestic animals in Luzon were limited to
Haematopinus tuberculatus (sucking louse of buffalo), Ctenocephalides felis (cat
flea), Rhipicephalus sanguineus (brown dog tick) and R. microplus (tropical
cattle tick) (Wolf 2010). Avian lice species documented
from domestic chickens in the country were M.
gallinae, L. caponis, M. pallidullus, G. dissimilis, and
O. dentatus (Manuel and
Anceno 1981).

Studies that address identification and distribution of
parasite fauna in remote regions of developing countries, like in Leyte Island,
are very limited and not given enough attention. Given their ability to transmit
dreadful human and animal diseases, the need for profiling is therefore urgent.
Ectoparasites distribution and taxonomic compositions are key points to
improve the diagnosis, prevention and control programs in an area for zoonotic
pathogens, as well as for economically important vector-borne diseases
(Fuehrer et al 2012). Hence, this paper presents a list of morphologically
identified ectoparasites from different animals in Baybay, Leyte, Philippines.

Materials and Methods

Study Area

The study was carried out in Baybay, Leyte Island which is
located in the eastern Visayas, central part of the Philippines at coordinate
10.6521412 °N, 124.8525626 °E. The climate is characterized by high humidity
(80-90%) and temperature (27.2 to 28.2°C). There’s no seasonal demarcation in
the area, but possessed high rainfall throughout the year (annual average =
2,500 mm). The eastern part is forested and highly elevated with gradual
decrease in elevation to the west towards the shore. Farming and fishing are the
two common livelihood of the local people, though some are involved in hunting
and collecting forest resources (LGU-Baybay 2013).

Parasite Collection, Preparation and Identification

Ectoparasites were collected in different villages of
Baybay, Leyte, Philippines and processed at the Parasitology Laboratory of the
College of Veterinary Medicine, Visayas State University. External parasites
were removed manually from the body of the host using forceps and placed in
vials containing Alcohol-Formalin-Acetic acid (AFA) for preservation.
Afterwards, they were processed and mounted in the slide following the technique
described by previous studies (Eduardo 2012; Palma 1978). Identification of the
parasite to the genus and species level was carried out using holistic approach,
which includes the parasitized hosts, location and finally the morphological key
of ectoparasite identification (Wall and Shearer 1997; Pratt and Stojanovich
1992; Stojanovich and Pratt 1992; Soulsby 1982; Emerson 1956).

Results

A total number of 577 ectoparasite were collected from
avian, ruminant, swine, canine, feline and reptile in Baybay, Leyte, Philippines
(Table 1). This constitutes 322, 71 and 184 numbers of lice, fleas and ticks,
respectively. We have identified a total of 19 different species (lice = 14
species; fleas= 2 species; and ticks = 3 species).

Lice (Phthiraptera)

Among the 322 number of lice, 14 species were
morphologically identified with 11 chewing type (8 species from order
Ischnocera; and 3 species from order Amblycera), and 3 sucking type (order
Anoplura). Chewing type lice were mainly observed in avian hosts, whereas
sucking type lice were only seen in mammalian. Species of chewing lice found to
infest chickens in the study area were Goniocotes gallinae (n=6), Goniodes
dissimilis (n=4), Lipeurus caponis (n=24), Oxylipeurus dentatus (n=25),
Menopon
gallinae (n=15), and Menacanthus stramineus (n=10) (Fig. 1). Large numbers of
ectoparasite in chicken were identified as L. caponis and O. dentatus.
Columbicola columbae (n=50) and Chelopistes meleagridis (n=6), which are both
chewing lice, were observed from rock pigeon and turkey, respectively.

In mammalian host, 3 species of chewing lice and 2 species
of sucking lice were identified. Goats were infested by Damalinia caprae (n=21)
and Linognathus spp. (n=23). Sheep were solely infested by D. ovis (n= 19),
while dogs were infested by Heterodoxus spinigera (n=32). Furthermore, the
sucking louse of buffalo (H. tuberculatus) were found in both carabao (n=70) and
cattle (n=12). In pigs, H. suis (n=5) was observed (Fig. 2).

Fleas (Siphonaptera)

The study has found 71 numbers of fleas infesting dogs and
cats, these are Ctenocephalides felis (n=70) and Pulex irritans (n=1) (Table 1).
Majority of the fleas were C. felis which was found to infest both dogs
and cats. Pulex irritans (human flea) was recorded in dog (Fig 3). On the other
hand, the study was not able to find C. canis.

Ticks (Ixodida)

A total of 184 hard ticks from 3 different species were
found in dogs, cattle, carabao and reticulated python (Table 1). Brown dog ticks
(Rhipicephalus sanguineus) (n=93) were the only species identified in dogs. The
tropical cattle ticks (R. microplus) (n=89) were found in both cattle and
carabao. The study has found Aponomma spp. (n=2) in reticulated python (Fig. 4).

Table 1. List
of species of lice, fleas and ticks found in domestic and exotic
animals in Baybay, Leyte, Philippines.

Discussion

The present list of ectoparasite under the orders
Pthiraptera (lice) and Siphonaptera (fleas), and suborder Ixodida (ticks) were
identified based on holistic approach, taking into account initially the host
and location where
the parasites were collected, and finally according to morphological keys for
diagnosis published by different authors (Wall and Shearer 1997; Pratt and
Stojanovich 1992; Stojanovich and Pratt 1992; Soulsby 1982; Emerson, 1956).
Identifying parasites in holistic way usually give an efficient process and
reliable result when confirmed by microscopy. Through this, morphological
identification becomes straightforward.

The present study reported 8 species of avian lice from
Baybay, Leyte, Philippines (Figure 1). Lice identified from chicken confirms the
study of Manuel and Anceno (1981) who reported M. gallinae, L. caponis,
M.
pallidullus, G. dissimilis, and O. dentatus in northern Philippines.
Interestingly, common lice from domestic chickens such as M. stramineus,
Goniodes spp., Goniocotes spp., M. gallinae and L. caponis were
observed in wild birds kept in rescue center in Quezon City, Philippines (Sia Su
et al 2013) despite the relative host specificity of many lice species. Though
this is possible when wild birds are in contact with infested chickens since the
degree of host specificity among lice is dictated by its ability to disperse
among multiple host species (Brooke and Nakamura 1998). Furthermore, 3 lice
species (L. caponis, G. dissimilis and M. gallinae)) observed in Tak Province,
Thailand were also observed in the study area (Changbunjong et al 2009). We have
identified C. columbae as main lice infesting rock pigeons and C. meleagridis
infesting turkey. Their occurrence has also been reported in many parts of the
world causing host debilitation (Galloway and Lamb 2015; Radfar et al 2011).

The identified lice from ruminants include D. caprae, D.
ovis, H. tuberculatus, Linognathus spp. and H. spinigera. In the Philippines,
other species of Damalinia was found to infest Philippine deer (Eduardo 2000)
and H. tuberculatus usually infest carabao (Del Rosario and Manuel 1983). In
terms of public health concern, a study conducted by Wolf (2010) showed that H.
tuberculatus collected from carabao in Luzon was positive for Rickettsia felis,
the causative agent of human spotted fever. We also recorded another sucking
louse (Linognathus spp.) that infests goat. This ectoparasite morphologically
differ from Haematopinus by the presence of smaller first pair of legs with
stout claws compared to the second and third pairs (Wall and Shearer, 1997). The
three known lice to infest dogs are Linognathus setosus, Trichodectes canis and
H. spinigera. According to Thompson (1939), it is rare to find these 3 species
co-occurring in one dog. However, there’s a great chance that the occurrence of
H. spinigera in dogs in Southeast Asian countries will persist due to better
lice adaptability, increase population of stray dogs, and pet popularity (Irwin
and Jefferies 2004).

Two species of fleas were recorded in our study. We found
C. felis in both dog and cat, and P. irritans in dogs. Dogs are not the common
host of the two identified fleas. C. felis is more common in cat. Similarly,
P.
irritans (human flea) infest mainly pigs and jump to human in contact. Indeed,
fleas are facultative parasites capable of infesting multiple host. A study in
Israel showed that these two species could transmit zoonotic diseases such as
Bartonella risking human having pet dogs (Sofer et al 2015). In fact, fleas are
transmitter of numerous parasites, bacteria and virus to animals and humans
(Bowman 2009).

In Southeast Asia, R. sanguineus and R. microplus are the
most common ticks in dog and large ruminant, respectively (Changbunjong et al
2009). While in reptiles, Aponomma spp. has also been recorded some Asian
countries (Petney et al 2007). Likewise, our study found these three species
infesting dog, ruminant and reticulated python. In central Philippines, R.
sanguineus and R. microplus were reported to carry
zoonotic microorganisms (e.g.
Anaplasma platys) (Ybañez et al 2012).
Also, Aponomma spp. has been reported
to transmit the pathogens Cowdria and Rickettsia, which causes Heartwater
disease in ruminant and spotted fever in human, respectively (Burridge et al
2000).

The result of our study offers the first list of
ectoparasite fauna in Baybay, Leyte, Philippines. Knowing their distribution and
taxonomic composition means a better understanding in terms of diagnosis,
prevention and control of vector and vector-borne diseases. Further studies are
needed to evaluate their spatiotemporal pattern and analyse its direct impact to
animals and human in remote and agricultural regions of the country.

Acknowledgement

We thank the owner of the animals and the clinicians/staff
of the College of Veterinary Medicine, Visayas State University for the
cooperation and assistance during the conduct of the study.

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